The barriers to whole-grain consumption among Iranian students

Studies show that regularly consuming whole grains reduce the risk of obesity and a wide range of chronic diseases. Despite this, studies reveal that students are consuming fewer whole grains. In the present study, we aimed to investigate the barriers to the consumption of whole grains among Iranian students. This cross-sectional study examined students at Fasa, Iran in 2020–2021. The online questionnaires were completed by students after receiving informed consent. Statistical analysis was performed using SPSS 26 and Chi-square, t-test, and logistic regression (P > 0.05). The current study involved 1890 students (1287 (68.1%) girls and 603 (31.9%) boys). Despite the preference for white flour bread among 53.8% of all students, 77.4% ate other whole-grain products, and 75.2% consumed all products at least once a week. Additionally, barriers such as access issues (70.5%), family supply issues (91.8%), lack appeal (72.8%), non-consumption by classmates (96.2%), and high prices in recent years (43.9%) were identified as obstacles to whole grain consumption. Furthermore, white bread eating students had significantly lower appetite levels and tended to eat fast food more often than those who ate whole grains (P < 0.05). We found that slightly more than half of the participants preferred to eat bread prepared with refined flour. Several other factors, including lack of access, lack of attractiveness, product price, parents not purchasing whole-grain products, students not paying attention to nutrition labels, peers’ effect, and eating with friends instead of family, also contribute to students avoiding whole-grain products.


Results
Participating in the study were 1890 students, including 1287 girls (68.1%) and 603 boys (31.9%). Details of the demographic and anthropometric information of the study population are listed in Table 1. Table 2 shows the results of the whole grain barriers questionnaire. According to this table, more than half of all students (53.8%) consumed white-flour bread, and this percentage in both girls and boys was higher than that of students who preferred to eat whole-grain bread.
Students also were asked about the benefits of eating whole grains. Although a higher percentage of all students (58.8%) considered whole grains as a source of fiber, it seems that most students did not have enough information on other benefits of whole-grain products such as a source of energy for a longer time (62.7%), www.nature.com/scientificreports/ supplier of vitamins and minerals (60.7%), and prevention of non-communicable diseases such as hypertension (86.7%), cancer (87.5%), type 2 diabetes (79.8%), and cardiovascular diseases (72.8%) ( Table 2). We also found that although a higher percentage of students preferred white bread, a significant percentage of students (77.4%) responded affirmative to the question, "Have you ever tried/eaten other whole-grain products?". We also revealed that 75.2% of all students reported consuming whole-grain products at least once or more per week. However, 29.7% of students did not consume whole-grain products at all (Table 2). Table 2 also shows that the barriers to consuming whole grain, include not availability (70.5%), didn't provide by parents or not having enough variety (91.8%), and not appealing (72.8%). Furthermore, the majority (96.2%) claimed that since their classmates did not consume these products, they did not want to. The matters about the price of whole-grain products and the effect of television also are displayed in this table. Additionally, about 74% of students responded positively to the question of "Do you think you will start eating or increase your whole grain consumption in the future?" and about 59% said that if whole-grain products are available in abundance, they prefer to consume them rather than white-flour products. Moreover, 76.5% of students reported that they would be more likely to eat whole grains if they ate more meals with their family rather than with friends. Furthermore, many (71.1% of the respondents) indicated that even if whole-grain products are not tasty, they would consume them due to their health benefits ( Table 2).
In Table 3, the type of bread and the number of times consumed whole-grain products did not differ significantly between girls and boys (P = 0.8 and P = 0.76, respectively). Furthermore, these differences were not statistically significant across educational levels (P = 0.79 and P = 0.98). There was no significant difference found between age and type of bread consumed or frequency of consumption of whole-grain products (P = 0.4 and P = 0.9).
This study found a relation between the type of bread consumed and the qualitative status of iron deficiency anemia. The relationship held even after adjusting the data (P < 0.05) ( Table 4). White flour consumption also resulted in significantly higher rates of nausea and vomiting (OR 2,08, 95% CI 1.08-4), gastroesophageal reflux (OR 2, 95% CI 1.02-3.33), and heartburn (OR 1.52, 95% CI 1.11-2.07) than whole-bread consumption (P < 0.05) ( Table 4). The relationship between these factors was held even after adjusting the data (P < 0.05).  www.nature.com/scientificreports/ According to Table 4, those who ate white or refined bread significantly skipped meals and snacks more than those who consumed whole-grain bread (P < 0.05). In this regard, students who ate more white bread were 1.3 times more likely to skip breakfast (OR 1.39, 95% CI 1.13-1.69), and this was also true for skipping other meals and snacks, even after adjusting the data (P < 0.05). Lastly, we found that whole-grain bread consumers were significantly more active (after adjusting the data) than students who ate refined grains (P < 0.05). In addition, Supplementary Table 1 shows that the relationships observed above are also valid for the frequency of consumption of whole grains (apart from the variables related to the elimination of meals and snacks).
As can be seen in Table 5, white flour consumption is associated with a significantly lower appetite (based on CNAQ) and this variable remains significant after adjusting data (P < 0.001). VAS data also support this association (P < 0.001). In addition, our analysis showed that white flour consumers are significantly more likely to consume junk foods (P = 0.001), fast food (P = 0.025) and soft drinks (P = 0.002) (even after adjusting the data). Additionally, we found that whole-grain bread consumers spent significantly less time to fall asleep (P = 0.003). Table 4. The relationship between the qualitative status of iron deficiency anemia, digestive problems, dietary pattern, and level of physical activity with the type of bread in the students. BMI, Body mass index. www.nature.com/scientificreports/ In addition, the frequency of consumption of whole grains was significantly related to appetite level (both VAS and CNAQ), (P = 0.005) and (P = 0.009) respectively) (Supplementary Table 2).

Discussion
Results of our study demonstrate that a higher percentage of students prefer white bread and that a significant portion of the participants was unaware of the benefits of eating whole grains. Furthermore, we discovered that about one-third of students did not consume any whole-grain products, and that approximately two-thirds did not find whole-grain products appealing or available.
The results of our study suggest that consumers may not consume whole grains for several reasons, including lack of availability, unattractiveness, and high price compared to products made with white flour. Other studies cite many factors as a poor whole-grain intake and a reluctance of students to consume whole grains. These factors include being a girl, lower household income, lack of awareness of the health benefits, household eating habits, difficulty identifying foods containing whole grains due to misleading labels, dislike of the taste, texture, and appearance of these foods, lack of availability, and their higher price than refined grains 7,21,26,27 . As children and adolescents dislike bitter foods, and whole-grain foods may be a little bitter, this may be one of the reasons why this group is hesitant to consume whole grains 28 . Due to its darker color as well as its coarser texture can also negatively impact school children's consumption of whole grains 28 . Another study suggests that one of the reasons students do not eat whole grains is that many households do not know how to cook whole-grain products 26 . All of these factors lead students to avoid products that contain whole grains, and therefore, consume products that contain refined grains.
In Iran, a study that directly examined the barriers to consume whole grains was not found based on our search. However, other research stated that many factors contribute to following an unhealthy diet pattern, especially among students. Among these factors, we can refer to the residence in populous and large cities such as Tehran; differences in social norms in recent years; less consumption of traditional dietary patterns that contain enough cereals and legumes, especially among the younger generation; more consumption of calorie-dense foods such as fast food and soft drinks; lower household income; low socioeconomic status; low level of education; smoking; low level of physical activity and having a sedentary lifestyle; less consumption of fruit, vegetables and fiber-rich foods; low level of parents' literacy and nutritional knowledge; consumption of white rice as a staple food and also white bread or refined grains as the main dietary component; high consumption of saturated oil; high salt intake; lack of appropriate food labeling; failure to raise public knowledge through media; high prevalence of eating disorder among adolescents; skipping breakfast as a mean meal for consuming whole grain; and type of food that friends and peers' choosing 13,14,[29][30][31][32][33][34] .
Income plays a crucial role in the field. According to our study, about 39 percent of study participants reported that whole-grain products are more expensive than white flour, and about 44 percent reported that prices have risen recently. A study that evaluated the trend of whole-grain consumption among adolescents in the United States between 2005 and 2012 found that although consumption of whole grains has increased significantly in high-income households, this increase was not observed in low-income households 26 . Despite this, the increase in high-income households was still much lower than the recommended amount for health 26 . According to this study, low-income households may not take the risk of buying food whose taste is not compatible with their favorite 26 . Therefore, perhaps government support and the lowering of the price of whole-grain products can increase the desire of all categories, especially students, to consume these products.
We observed in the present study that one of the reasons for people not consuming whole grains is lack of knowledge about their benefits. School-aged children were unaware of the benefits of whole grains, such as providing energy for longer periods and supplying vitamins and minerals. Additionally, many did not aware of the fact that eating whole grains can prevent many non-communicable diseases. Other studies have shown contradictory results. Although some studies suggest that the reason for reduced whole-grain consumption is lack of knowledge about the benefits of these products 11 , one study states that many adolescents are aware of the www.nature.com/scientificreports/ benefits of whole-grain foods, regardless of which specific disease is associated with low consumption of whole grains (7). According to another study, whole-grain consumption can be increased by properly educating people about health benefits 35 . Therefore, students and their parents might be more likely to consume whole grains if they are aware of what whole grains can do. Based on the findings of the present study, age, gender, and educational level were not associated with the type of bread consumed or the frequency of consuming whole-grain products. Previous studies have reported contradictory results. Similarly, it has been demonstrated in some studies that gender is not associated with whole grain consumption 27 . By contrast, according to a UK study, young people (under 18 years old) consume a very low level of whole grains, with an average of only 7 g per day 36 . In addition, approximately half of the participants in the 7-day evaluation did not consume any whole-grain breakfast cereals, but this ratio significantly increased with age 36 . The rate of non-consumption of whole grains increased with age, according to another study conducted in the United States 37 . These differences can be explained by the different populations studied.
Our study results showed that students who ate white bread were 1.3 times more likely to skip breakfast, other meals, and snacks than those who ate whole-grain bread. Breakfast is a very important meal, so its' absence can contribute to academic failure 38 . In a UK study, 15-to 18-year-old girls reported the lowest intake of whole grains for breakfast, which might be the result of teens skipping breakfast 36 . In addition, the study found that the major sources of whole grains consumed by British teenagers were breakfast cereals and bread, although half of the students refused to eat breakfast cereals containing whole grains and three-quarters refused to eat wholemeal bread 36 . Similar results have been reported in the USA 11,37 . These studies may not be comparable, as they were conducted in different years and different regions, as well as varying methodologies and lengths of time. In addition to this, the definition of whole grains and the recommended daily amount vary from country to country. It could also be a contributing factor that the results of this study differ from those of other studies since consumption of ready-to-eat cereals among Iranians are not common for breakfast, as opposed to other countries where these products are the most common source of whole grains 7 .
Our research showed that school-aged children who ate more white bread reported significantly more digestive problems such as nausea and vomiting, reflux, and heartburn. Several studies identified that eating whole grains can improve digestive problems such as heartburn, bloating, and irritable bowel syndrome 39 . In this study, we also found that students who ate white bread had significantly fewer appetites but consumed more soda and fast food. In this regard, some studies have found that adolescents who consume whole grain have a lower tendency to consume fast food 21 . On the other hand, a meta-analysis study found that consumption of whole grains versus refined grains significantly affected subjective appetite and, consequently, consumption of whole grains reduced the risk of overweight and obesity 40 . It seems that more research is needed in this area.
Adolescents' consumption of whole grains is influenced by individual, family and environmental factors 41,42 . Accordingly, we observed that students who ate more meals with their families instead of eating with friends were more likely to consume whole-grain products. In addition, we noted that 96% of students feel hesitant to consume such products because their peers do not consume them. Similarly, a study found that the availability of whole-grain foods at home or at school can have a positive effect on adolescents' consumption of whole grains throughout the day 27 . According to this study, one of the best ways to use whole-grain products at home is to use products that require the least preparation and cooking time 27 . Based on another study, adolescents share a lot of eating patterns with their friends, and whole-grain consumption was found to be associated positively with close friendships 43 . Furthermore, a study found that adolescents are influenced by their families in their food choices, which can change their attitude toward healthy eating and whole grains 44 . It may be possible to increase the intake of whole grains among students by controlling these factors, which have a considerable impact on their consumption or non-consumption of whole grains.
According to our study, about 40% of the study population failed to pay attention to nutrition labels when purchasing foods. Another study shows that adolescents have difficulty identifying whole-grain products 7 . The problem with whole-grain products in this respect is that whole grain labels vary from country to country and also the minerals and fiber levels of such products vary due to growing and soil conditions so that consumers cannot identify such products correctly 7,9,19 . In addition, recommendations for the consumption of whole-grain products vary from region to region and country to country and also there are different definitions of the amount of whole-grain products required for a healthy diet 1,23,45 . Generally, a whole-grain food contains at least 8 g of whole grains per 30 g of product, according to the American Association of Cereal Chemists International. In this definition, 30 g is considered as a standard serving of whole-grain products 46 . In contrast, epidemiological studies have introduced the arbitrary value of 25% of cereal breakfast as whole-grain food, due to the consumption of whole grains and the risk of non-communicable diseases 9,47 . According to another FDA definition, a product is considered a whole grain if it contains at least 51% whole grain ingredient(s) (by weight) per reference 9 . As a result, disagreements over the definition of whole grains confuse the community and create uncertainty for producers of products containing whole grains. Consumers, on the other hand, did not specify which products they considered rich in whole grains 7 . Thus, it may be possible to reduce this confusion in society by defining a whole grain product in one way and encouraging all groups, especially students, to consume them.
Even though we did not find a significant relationship between BMI and consumption of whole grain bread in the present study, our findings showed that consumers of whole grain bread were significantly more active. This can be explained by the fact that a person who consumes whole-grain products maybe is more committed to a healthy lifestyle and therefore has a higher level of physical activity. While the results of a study conducted in United States were similar to ours and they showed that consumption of whole grains was not associated with BMI 20 , other studies suggest otherwise. In this regard, other investigations have shown that whole grains can significantly prevent overweight and obesity, especially in students 40,48 . A study also conducted in the United States determined that consumption of more than 3 servings of whole grains in children 6 to 12 years old was not associated with control of overweight and obesity in this age group, whereas consumption of 1.5 to 3 servings www.nature.com/scientificreports/ of whole grains per day was positively and significantly associated with weight measures. Additionally, the BMI z-score in this study was significantly lower in adolescents aged 13 to 18 years who consumed the most whole grains during the day 19 . In another study, adolescent boys who ate whole grains for breakfast had a significantly lower risk of obesity 49 . The explanation for these differences could be under-reporting, sociodemographic factors, or dietary patterns prevalent in the study population. Furthermore, the duration of the intervention varies from study to study, resulting in conflicting results. According to our results, despite the fact that whole grain products were not tasty, a significant percentage of students were willing to eat them for health benefits. Meanwhile, we observed that about half of the students said they were familiar with whole grains because of television. Social media has been shown to encourage more students to consume whole grains in other studies 44 . Therefore, by raising awareness, it may be possible to increase the consumption of whole grains among adolescents. Other suggestions for increasing whole grain consumption among students include (1) consuming fast food with pieces of bread made from whole grains; (2) cheaper prices of products containing whole grains than refined grains; (3) TV advertising the consumption of whole grains; (4) improving the taste of whole-grain products using existing technologies; (5) free snacks for students that contain whole grains. Other studies in this area include suggestions such as advertising, increasing the sensory appeal of whole-grain products, abundant availability in schools and stores, formulation of new foods, snacks higher in fiber content, lowering prices, conducting educational campaigns and tailoring products to young people, and improving labeling to encourage more students to consume whole-grain products 7,23 .
Although this study examined a significant population, it had some limitations. First, the economic status of student households was not evaluated, and this should be considered in future research. Second, because of the nature of the study, a causal relationship could not be established. Another limitation of this study is that the data was collected online and through self-reporting, meaning that there is a possibility of reporting errors. Iron deficiency anemia was also evaluated qualitatively in the present study, which recommends future studies should use clinical tests. It is suggested that longitudinal studies be conducted in the future to determine what factors prevent students from consuming whole grains.

Conclusion
This study examined barriers to the consumption of whole grains among Iranian students for the first time. Approximately half of the participants in our study preferred to consume bread made with refined flour. This could be explained by the fact that students are unaware of the benefits of using whole grains, as, a significant number of students were not aware that whole grains have many health benefits. According to the current study, several other barriers prevent students from consuming whole-grain products, including lack of access, lack of attractiveness, products price, parents not buying whole-grain products, don't enough attention to nutrition labels by students, peers' effect, and eating with friends instead of family. Furthermore, encouraging students to eat breakfast can also help them consume more whole grains, since breakfast is an important step for improving whole grain consumption. As a result, television and other social media can influence students to consume more whole-grain products. In conclusion, while we need more studies, particularly longitudinal or prospective studies, to better understand this issue, policymakers can use the results of this study and the proposed solutions to increase whole grain consumption among students. The chance of the burden of future chronic diseases in society may be reduced in part by adopting such an approach.

Methods
This cross-sectional study was conducted from 2020 to 2021 among Iranian students covered by Fasa Education Department. Fasa is located in Fars Province and southwestern Iran. It has a population of about 250,000 according to the most recent census. This study is part of the plan to control overweight and obesity in students, and the contact numbers of students were provided to us by the Fasa Education Department. In this research, first, study participants were sent an informed consent form online. If they wished to participate in the study and filled out the informed consent, they were given the phone number and address of the project manager so that they could easily contact us if they had any questions. After receipt of online informed consent, demographic and anthropometric checklist, the 8-item Council of Nutrition Appetite Questionnaire (CNAQ) 50 , physical activity questionnaire, and a modified questionnaire on barriers to whole grain intake 7 were completed online by students. It is worth mentioning that the barriers to whole-grain consumption questionnaire was based on the Kamar et al. 7 questionnaire, but the students were asked to choose multiple-choice answers for easier answering.
A demographic checklist included factors such as age, sex, education level, height, weight, waist, and wrist circumference. Students were clearly explained how to measure anthropometric indices through a video submitted. Body mass index (BMI) was calculated by dividing weight (kg) by height squared (cm). The next questionnaire measures barriers to consuming whole grains by asking questions about the level of knowledge, attitude, desire to consume whole grains, and frequency of consumption. Also it included questions about what prevents students from consuming whole grains 7 . These questions are listed separately in Table 2.
In the current study, since bread is considered as staple food in Iran, the consumption of whole grains or white flour was evaluated by the consumption of type of bread. In the CNAQ, responses are scored based on a 5-point scale (A to E) (A = 1, B = 2, C = 3, D = 4, E = 5) and the final score evaluates the appetite. This questionnaire is scored on a scale from 8 (minimum) to 40 (maximum) 50 . It is noteworthy to mention that the psychometric properties of CNAQ was assessed in the USA which significantly correlated with the total score of the appetite hunger and sensory perception questionnaire (AHSP) and its sub-domain. CANQ also had Cronbach's alpha equal to 0.72 50 . It should be noted that in addition to the appetite questionnaire, visual analog scales (VAS) were also evaluated in the present study. VAS is an anchor term that is recognized as a method for assessing changes in appetite over time 40 . This questionnaire is graded on a scale from zero to ten, with zero indicating no appetite www.nature.com/scientificreports/ and 10 indicating the highest degree of appetite. The physical activity questionnaire also uses 3 questions to calculate a person's exercise habits and level of physical activity. These questions assess the frequency, intensity, and duration of physical activity, and when these three items are multiplied together, the level of physical activity is obtained. The final score of this questionnaire can vary from less than 20 (sedentary) to more than 81 (very active) 51 . In the final analysis, we divided people into four groups: sedentary, low-activity (not good enough), moderately active (acceptable but could be better), and active or very active. This questionnaire has been also validated by previous studies 51,52 . The students were also asked about their dietary patterns and how to eat fast food by way of an online form, as well as questions about gastrointestinal diseases. During this study, the qualitative status of iron deficiency anemia was assessed through the checklist. This checklist included three questions, and it was based on the most important symptoms of iron deficiency anemia. The answer to these questions was either yes or no. The questions are presented in Table 4. Moreover, the quality of sleep based on how much sleep was given during 24 h a day and the length of time it took for the student to fall asleep. The questionnaire was sent to each student via their smartphones as a link due to the prevalence of Coronavirus disease (COVID-19). Notably, for students who were not able to answer or fully understand the questions due to their young age (first to fourth grade), the information was provided by a first-degree relative who lived with the student or who have accurate information from the student's circumstances.
In the present study, the inclusion criteria included all students from all educational levels who wanted to complete the questionnaire online. Exclusion criteria included: unwillingness to participate in the study, special diets such as vegetarianism, extreme disability such that the student is unable to respond, psychotic mental illness, diseases leading to lack of recall (such as Alzheimer's disease), gastrointestinal diseases such as celiac disease, autoimmune diseases such as multiple sclerosis, and a variety of cancers. It should be noted that as this project was conducted through an online call, all students who participated in the project were studied. The consent form and questionnaires were sent online to about 25,000 students and those who were interested, filled out the questionnaire and participated. It is necessary to mention that the study protocol was in accordance with the Declaration of Helsinki guidelines and was approved by the Institutional Review Board (IRB) of the Fasa University of Medical Sciences (Code: IR.FUMS.REC.1400.158).

Statistical analysis.
Results were presented as mean and standard deviation. A Chi-square test was used to compare qualitative variables. Independent t-tests were used to compare quantitative variables. The effect of confounding variables was eliminated by multivariate logistic regression. This model reported significance and odds ratio along with a 95% confidence interval. Calculations were performed using SPSS version 26. Probabilities less than 0.05 were considered significant.
Ethical approval and consent to participate. The study protocol was following the Helsinki Declaration and was confirmed by the Ethics Committee of Fasa University of Medical Sciences (Approval Code: IR.FUMS.REC.1400.158). The participants were informed about the research objectives and a consent form through online was obtained from the subjects before starting the survey.

Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request to the corresponding author.